Phylogenetic analysis of the ATP-binding cassette proteins suggests a new ABC protein subfamily J in Aedes aegypti (Diptera: Culicidae)

- Phylogenetic analysis of the ATP-binding cassette proteins suggests a new ABC protein subfamily J in Aedes aegypti (Diptera: Culicidae).
- Background: We performed an in-depth analysis of the ABC gene family in Aedes aegypti (Diptera: Culicidae), which is an important vector species of arthropod-borne viral infections such as chikungunya, dengue, and Zika..
- Despite its importance, previous studies of the Arthropod ABC family have not focused on this species.
- Results: We identified 53 classic complete ABC proteins annotated in the A.
- A phylogenetic analysis of Aedes aegypti ABC proteins was carried out to assign the novel proteins to the ABC subfamilies.
- We also determined 9 full-length sequences of DNA repair (MutS, RAD50) and structural maintenance of chromosome (SMC) proteins that contain the ABC signature..
- Conclusions: After inclusion of the putative ABC proteins into the evolutionary tree of the gene family, we classified A.
- aegypti ABC proteins into the established subfamilies (A to H), but the phylogenetic positioning of MutS, RAD50 and SMC proteins among ABC subfamilies — as well as the highly supported grouping of RAD50 and SMC — prompted us to name a new J subfamily of A.
- aegypti ABC proteins..
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- Among these processes, the ABC transporters are mostly involved in extra and intra- cellular trans membrane ATP energy driven traffic of molecules such as lipids, amino acids, hormones and xenobiotics [2, 3]..
- The TMD domains of the ABC- transporters are composed of five to ten membrane- spanning regions that are involved in substrate trans- location.
- The traditional classification is based on sequence similarity and arranged the ABC protein diversity into eight subfamilies (A- H) [6].
- The ABCE and ABCF sub- families are unique among the ABC proteins because they exhibit a pair of linked nucleotide-binding domains while lacking trans membrane domains [3, 6].
- Plants, besides presenting eukaryotic ABC subfamilies A to G, exhibit a heteroge- neous and extensive group of ABC proteins that bear similarities to the components of prokaryotic multi- subunit ABC transporters.
- Three other groups of proteins not assigned to the subfamilies mentioned above exhibit ABC transporter domains: (1) the MutS proteins that are responsible for DNA mismatch repair and maintenance of genomic sta- bility [11, 12].
- Although MutS, SMC, and Rad50 proteins show ABC protein characteristics, they have not yet been included in the standard ABC classification for humans, arthropods, and the Caenorhabditis elegans nematode .
- Nonetheless, in the complete inventory of ABC proteins of the Arabidopsis thaliana plant, SMC proteins were pro- posed as a new ABC protein subfamily [17]..
- Some ABC proteins have been associated with multidrug resistance (MDR) phenotype in a variety of organisms.
- and multiple resistance—when several coexisting defense mechanisms act in the same organism [24, 25]..
- Recent surveys of the ABC gene family in arthropods included the fruit fly Drosophila melanogaster, the mos- quito Anopheles gambiae, the beetle Tribolium casta- neum, the honey bee Apis mellifera, the silkmoth Bombyx mori, the water flea Daphia pulex, and the spider mite Tetranychus urticae [16].
- By includ- ing all the putative proteins that exhibit the ABC domain into a phylogenetic analysis, we showed that SMC, Rad 50, and MutS proteins were part of the main.
- ABC gene family diversification, which justifies the prop- osition of a new subfamily of the ABC proteins..
- aegypti genome retrieved 62 complete proteins that were identified as ABC trans- porters when submitted to the NCBI Conserved Domain Database.
- The ABC gene family phylogeny recovered subfamilies A-H with significant statistical support (Fig.
- The sizes of gene subfamilies varied significantly with subfamilies A-C and G consisting of the larger groups.
- The variation of the rate of evolution within each ABC subfamily as measured by the heterogeneity of the dis- tance between the common ancestor of all members of the subfamily and the tips was higher in subfamily.
- Surpris- ingly, root placement using the minimal ancestor deviation (MAD) method suggested that subfamily ABCG is a sister to the remaining ABC transporters in- cluding the clades consisting of SMC and Rad50 pro- teins as well as the MutS proteins that were positioned as a sister to subfamily ABCD (Fig.
- To investigate ABC transporters in the A.
- aegypti ABC transporters to investigate the assignment of the putative proteins to the described subfamilies of these trans- porters.
- We identified ten members of the A.
- 1 a Maximum likelihood phylogeny of the ABC gene family including SMC, Rad50 and MutS genes.
- Four mem- bers of this cluster have genes organized in tandem in the supercontig 1.726, two members belong to the supercontig 1.321, and four belong to other supercontigs (Table 2).
- aegypti genome were assigned to the ABCB subfamily (Fig.
- This subfamily is composed of putative homologs of the human P-glycoprotein, which plays key physiological roles such as the excretion of toxic compounds and the multidrug resistance phenotype .
- melanoga- ster protein classified as belonging to the ABCB (CG31792_B) subfamily was recovered in the ABCC clade.
- One of the most diverse subfamilies identified in the mosquito genome was the ABCC with 15 members—all full transporters (Table 2).
- The ABCD and ABCE subfamilies were the least di- verse of the groups identified in humans—the former is known to appear as half transporters forming homo or heterodimers in peroxisomes acting in lipid transport .
- This was consistent with the findings of a single ABCE gene in the A.
- Like ABCE proteins, the ABCF subfamily also lacks the TMD and is involved in the ribosome complex formation and activation [46–48];.
- only three of these proteins were found in the mosquito genome in our analysis..
- Although only five members of the ABCG proteins were described in humans proteins belonging to this group were identified for A.
- aegypti mosquito is likely due to a series of duplication events that is supported by the tan- dem organization observed in the supercontig 1.337 of the A.
- Only one ortholog of the white and scarlet proteins was found in the A.
- aegypti genome but no ortholog of the brown protein was found.
- Here, four members of the ABCH subfamily were identi- fied in the A.
- New insights into insecticide ef- flux, ATP-dependent efflux pump inhibitors, and/or RNAi associated with pesticides will potentially assist in the development of control strategies for important vec- tors of infectious diseases like A.
- Notably, Rad50 has a relatively well- conserved LSGG motif compared to the classic ABC proteins.
- Table 1 Classification of ABC proteins subfamilies in Homo sapiens and Drosophila melanogaster.
- facilities dimerization of large molecules restoring the close proximity of the Walker A and B motifs for nu- cleotide binding [53].
- Finally, perhaps a distant lineage but still within the ABC diversification [55], are the DNA repair enzymes such as MutS [56]..
- These proteins form dimers and have a conserved mechanism of conformational change observed in the classic ABC proteins.
- The ATP binding and NBD dimerization promote changes in the substrate-binding domains that are important for the function of the ABC-type ATPases.
- The substrate- binding domains of the SMC and Rad50 proteins are lo- cated in similar positions as the classic ABC proteins [52].
- The ABC proteins subfamilies are grouped together based on sequence similarity and proteins belonging to the same subfamily usually have similar functions.
- Our results showed that ABC subfamilies were always strongly recovered in the gene family phylogeny and that the sequences of SMC and Rad50 proteins formed a well-supported clade (100 bootstrap support), sister to MutS proteins, and ABC transporters excluding ABCG..
- We know the following: (i) SMC and Rad50 pro- teins exhibit similar functions on DNA repair and chromosomal maintenance ii) they form a strongly supported clade with ABC trans- porters phylogeny, and (iii) they exhibit the structural and sequence characteristics of ABC proteins.
- Thus, we propose these proteins be included in the ABC gene family with the creation of a new subfamily called J (Fig.
- Table 2) that includes ABC proteins involved in DNA repair and structural maintenance of the chromosomes..
- In summary, we found 53 classic complete ABC pro- teins annotated in the A.
- We also found 9 sequences of the Rad, MutS, and SMC in the Aedes genome database that clustered with human and D.
- melanoga- ster orthologs in the same clade.
- Considering other similarities observed between these enzymes and the classic ABC proteins, we propose these proteins be included in the ABC gene family followed by creation of a new subfamily called J that includes ABC en- zymes involved in DNA repair and the structural maintenance of the chromosome..
- Table 1 Classification of ABC proteins subfamilies in Homo sapiens and Drosophila melanogaster (Continued).
- Table 2 Characterization of the 62 A.
- aegypti ABC proteins.
- AaegABCB1L/AaegP-gp AAEL010379-PA 1307 TMD1-NBD1-TMD2-NBD .
- All putative homologous sequences were submitted to the NCBI Conserved Domain Database [58, 59] to con- firm the presence of the ATP-binding cassette domain..
- coupled with ten relative rate classes to accommodate Table 2 Characterization of the 62 A.
- aegypti ABC proteins (Continued).
- Because no out- group was included in our analysis, rooting of the ABC gene genealogy was performed using the minimal ancestor deviation method of Tria at al.
- Rooting is necessary for establishing the chronological direction of the ABC gene family evolution (Supplemental material 4)..
- ABC.unrooted.txt: Unrooted maximum likelihood phylogenetic tree of the ABC gene family..
- We dedicate this paper to the memory of our friend Dr.
- The datasets analysed during the current study are available in the GenBank and VectorBase repositories.
- One of the authors (CGS) is a member of the editorial board for the BMC Genomics journal..
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